Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis

Abstract Ulcerative colitis (UC) is a refractory, chronic inflammatory bowel disease of unknown etiology. Although platelets are activated in UC, their relevance in pathophysiology remains unclear. We analyzed the correlation of platelet activation and platelet–monocyte complexes (PMCs) with severit...

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Main Authors: Yasuki Sano, Takashi Tomiyama, Naoto Yagi, Yuka Ito, Yusuke Honzawa, Tomomitsu Tahara, Tsukasa Ikeura, Toshiro Fukui, Shinji Shimoda, Makoto Naganuma
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-78462-8
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author Yasuki Sano
Takashi Tomiyama
Naoto Yagi
Yuka Ito
Yusuke Honzawa
Tomomitsu Tahara
Tsukasa Ikeura
Toshiro Fukui
Shinji Shimoda
Makoto Naganuma
author_facet Yasuki Sano
Takashi Tomiyama
Naoto Yagi
Yuka Ito
Yusuke Honzawa
Tomomitsu Tahara
Tsukasa Ikeura
Toshiro Fukui
Shinji Shimoda
Makoto Naganuma
author_sort Yasuki Sano
collection DOAJ
description Abstract Ulcerative colitis (UC) is a refractory, chronic inflammatory bowel disease of unknown etiology. Although platelets are activated in UC, their relevance in pathophysiology remains unclear. We analyzed the correlation of platelet activation and platelet–monocyte complexes (PMCs) with severity of mucosal inflammation using the Mayo endoscopic subscore (MES). Platelet activation marker, CD62P was upregulated in patients with UC compared with that in healthy controls (P < 0.05). CD62P expression was significantly higher in patients with MES3 (severe inflammation) than in those with MES ≤ 2 (endoscopic remission to moderate inflammation) (P < 0.001). The concentration of sCD62P in patients with MES0 (endoscopic remission) was significantly higher than in those with MES ≥ 1 (P < 0.01). The expression of CD40L, CD63, PAC-1, annexin V, and CD36, and the concentrations of sCD40L, PF4, and RANTES did not correlate with MES. The proportion of PMCs in patients with MES3 was higher than in those with MES ≤ 2 (P < 0.05). CD16 expression on monocytes with platelets was significantly higher than in monocytes without platelets (P < 0.001). Patients with complete remission after treatment showed significant reduction in PMCs 3 months after treatment (P < 0.05) but had no change in CD62P and sCD62P. Our data suggest that platelet activation via the CD62P–PMC axis is involved in UC pathophysiology.
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spelling doaj-art-eaaca6c71cd74988a097741dc4aa7c062024-11-17T12:30:01ZengNature PortfolioScientific Reports2045-23222024-11-0114111010.1038/s41598-024-78462-8Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitisYasuki Sano0Takashi Tomiyama1Naoto Yagi2Yuka Ito3Yusuke Honzawa4Tomomitsu Tahara5Tsukasa Ikeura6Toshiro Fukui7Shinji Shimoda8Makoto Naganuma9Third Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityThird Department of Internal Medicine, Division of Gastroenterology and Hepatology, Kansai Medical UniversityAbstract Ulcerative colitis (UC) is a refractory, chronic inflammatory bowel disease of unknown etiology. Although platelets are activated in UC, their relevance in pathophysiology remains unclear. We analyzed the correlation of platelet activation and platelet–monocyte complexes (PMCs) with severity of mucosal inflammation using the Mayo endoscopic subscore (MES). Platelet activation marker, CD62P was upregulated in patients with UC compared with that in healthy controls (P < 0.05). CD62P expression was significantly higher in patients with MES3 (severe inflammation) than in those with MES ≤ 2 (endoscopic remission to moderate inflammation) (P < 0.001). The concentration of sCD62P in patients with MES0 (endoscopic remission) was significantly higher than in those with MES ≥ 1 (P < 0.01). The expression of CD40L, CD63, PAC-1, annexin V, and CD36, and the concentrations of sCD40L, PF4, and RANTES did not correlate with MES. The proportion of PMCs in patients with MES3 was higher than in those with MES ≤ 2 (P < 0.05). CD16 expression on monocytes with platelets was significantly higher than in monocytes without platelets (P < 0.001). Patients with complete remission after treatment showed significant reduction in PMCs 3 months after treatment (P < 0.05) but had no change in CD62P and sCD62P. Our data suggest that platelet activation via the CD62P–PMC axis is involved in UC pathophysiology.https://doi.org/10.1038/s41598-024-78462-8Ulcerative colitisCD62PPlatelet–monocyte complexesMayo endoscopic subscoreCD16
spellingShingle Yasuki Sano
Takashi Tomiyama
Naoto Yagi
Yuka Ito
Yusuke Honzawa
Tomomitsu Tahara
Tsukasa Ikeura
Toshiro Fukui
Shinji Shimoda
Makoto Naganuma
Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
Scientific Reports
Ulcerative colitis
CD62P
Platelet–monocyte complexes
Mayo endoscopic subscore
CD16
title Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
title_full Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
title_fullStr Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
title_full_unstemmed Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
title_short Platelet activation through CD62P and the formation of platelet–monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
title_sort platelet activation through cd62p and the formation of platelet monocyte complexes are associated with the exacerbation of mucosal inflammation in patients with ulcerative colitis
topic Ulcerative colitis
CD62P
Platelet–monocyte complexes
Mayo endoscopic subscore
CD16
url https://doi.org/10.1038/s41598-024-78462-8
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AT takashitomiyama plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis
AT naotoyagi plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis
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AT yusukehonzawa plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis
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AT toshirofukui plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis
AT shinjishimoda plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis
AT makotonaganuma plateletactivationthroughcd62pandtheformationofplateletmonocytecomplexesareassociatedwiththeexacerbationofmucosalinflammationinpatientswithulcerativecolitis